Signal regulators of systemic acquired resistance

Frontiers in Plant Science

Volumn 6, Issue APR, 2015, Pages

  Gao, Qing Ming ^a   Zhu, Shifeng ^a,b   Kachroo, Pradeep ^a   Kachroo, Aardra ^a  

^a UNIVERSITY OF KENTUCKY   (United States)

^b NANKAI UNIVERSITY   (China)

Author keywords

Glycerol 3 phosphate; Lipids; Plant defense; Reactive oxygen species; Systemic resistance

Indexed keywords

EID: 84928160304     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2015.00228     Document Type: Article

References (175)

1. An, C., and Mou, Z. (2011). Salicylic acid and its function in plant immunity. J. Integr. Plant Biol. 53, 412–428. doi: 10.1111/j.1744-7909.2011.01043.x
2. Attaran, E., Zeier, T. E., Griebel, T., and Zeier, J. (2009). Methyl salicylate production and jasmonate signaling are not essential for systemic acquired resistance in Arabidopsis. Plant Cell 21, 954–971. doi: 10.1105/tpc.108.063164
3. Balmer, D., de Papajewski, D. V., Planchamp, C., Glauser, G., and Mauch-Mani, B. (2013). Induced resistance in maize is based on organ-specific defence responses. Plant J. 74, 213–225. doi: 10.1111/tpj.12114
4. Besson-Bard, A., Pugin, A., and Wendehenne, D. (2008). New insights into nitric oxide signaling in plants. Annu. Rev. Plant Biol. 59, 21–39. doi: 10.1146/annurev.arplant.59.032607.092830
5. Bhattacharjee, S., Halane, M. K., Kim, S. H., and Gassmann, W. (2011). Pathogen effectors target Arabidopsis EDS1 and alter its interactions with immune regulators. Science 334, 1405–1408. doi: 10.1126/science.1211592
6. Bogdanove, A. J., and Martin, G. B. (2000). AvrPto-dependent Pto-interacting proteins and AvrPto-interacting proteins in tomato. Proc. Natl. Acad. Sci. U.S.A. 97, 8836–8840. doi: 10.1073/pnas.97.16.8836
7. Bozkurt, T. O., Schornack, S., Win, J., Shindo, T., Ilyas, M., Oliva, R., et al. (2011). Phytophthora infestans effector AVRblb2 prevents secretion of a plant immune protease at the haustorial interface. Proc. Natl. Acad. Sci. U.S.A. 108, 20832–20837. doi: 10.1073/pnas.1112708109
8. Breitenbach, H. H., Wenig, M., Wittek, F., Jordá, L., Maldonado-Alconada, A. M., Sarioglu, H., et al. (2014). Contrasting roles of the apoplastic aspartyl protease apoplastic, enhanced disease susceptibility1-dependent1 and legume lectin-like protein1 in arabidopsis systemic acquired resistance. Plant Physiol. 165, 791–809. doi: 10.1104/pp.114.239665
9. Cacas, J. L., Petitot, A. S., Bernier, L., Estevan, J., Conejero, G., Mongrand, S., et al. (2011). Identification and characterization of the non-race specific disease resistance 1 (NDR1) orthologous protein in coffee. BMC Plant Biol. 11:144. doi: 10.1186/1471-2229-11-144
10. Caillaud, M. C., Piquerez, S. J., Fabro, G., Steinbrenner, J., Ishaque, N., Beynon, J., et al. (2012). Subcellular localization of the Hpa RxLR effector repertoire identifies a tonoplast-associated protein HaRxL17 that confers enhanced plant susceptibility. Plant J. 69, 252–265. doi: 10.1111/j.1365-313X.2011.04787.x
11. Cameron, R., Paiva, N. L., Lamb, C. J., and Dixon, R. A. (1999). Accumulation of salicylic acid and PR-1 gene transcripts in relation to the systemic acquired resistance (SAR) response induced by Pseudomonas syringae pv. Tomato in Arabidopsis. Physiol. Mol. Plant Pathol. 55, 121–130. doi: 10.1006/pmpp.1999.0214
12. Canet, J. V., Dobón, A., and Tornero, P. (2012). Non-recognition-of-BTH4, an Arabidopsis mediator subunit homolog, is necessary for development and response to salicylic acid. Plant Cell 24, 4220–4235. doi: 10.1105/tpc.112.103028
13. Century, K. S., Holub, E. B., and Staskawicz, B. J. (1995). NDR1, a locus of Arabidopsis thaliana that is required for disease resistance to both a bacterial and a fungal pathogen. Proc. Natl. Acad. Sci. U.S.A. 92, 6597–6601. doi: 10.1073/pnas.92.14.6597
14. Century, K. S., Shapiro, A. D., Repetti, P. P., Dahlbeck, D., Holub E., and Staskawicz, B. J. (1997). NDR1, a pathogen-induced component required for Arabidopsis disease resistance. Science 278, 1963–1965. doi: 10.1126/sci-ence.278.5345.1963
15. Cesari, S., Thillieza, G., Ribota, C., Chalvona, V., Michela, C., Jauneauc, A., et al. (2013). The rice resistance protein pair RGA4/RGA5 recognizes the magna-porthe oryzae effectors AVR-Pia and AVR1-CO39 by direct binding. Plant Cell 25, 1463–1481. doi: 10.1105/tpc.112.107201
16. Chanda, B., Xia, Y., Mandal, M. K., Sekine, K. T., Gao, Q. M., Selote, D., et al. (2011). Glycerol-3-phosphate is a critical mobile inducer of systemic immunity in plants. Nat. Genet. 43, 421–427. doi: 10.1038/ng.798
17. Chandra-Shekara, A. C., Gupte, M, Navarre, D., Raina, S., Raina, R., Klessig, D. F., et al. (2006). Light-dependent hypersensitive response and resistance signaling to turnip crinkle virus in Arabidopsis. Plant J. 45, 320–334. doi: 10.1111/j.1365-313X.2005.02618.x
18. Chandra-Shekara, A. C., Navarre, D., Kachroo, A., Kang, H. G., Klessig, D. F., and Kachroo, P. (2004). Signaling requirements and role of salicylic acid in HRT-and rrt-mediated resistance to turnip crinkle virus in Arabidopsis. Plant J. 40, 647–659. doi: 10.1111/j.1365-313X.2004.02241.x
19. Chandra-Shekara, A. C., Venugopal, S. C., Barman, S. R., Kachroo, A., and Kachroo, P. (2007). Plastidial fatty acid levels regulate resistance gene-dependent defense signaling in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 104, 7277–7282. doi: 10.1073/pnas.0609259104
20. Chaturvedi, R., Krothapalli, K., Makandar, R., Nandi, A., Sparks, A., Roth, M., et al. (2008). Plastid omega3-fatty acid desaturase-dependent accumulation of a systemic acquired resistance inducing activity in petiole exudates of Arabidopsis thaliana is independent of jasmonic acid. Plant J. 54, 106–117. doi: 10.1111/j.1365-313X.2007.03400.x
21. Chaturvedi, R., Venables, B., Petros, R. A., Nalam, V., Li, M., Wang, X., et al. (2012). An abietane diterpenoid is a potent activator of systemic acquired resistance. Plant J. 71, 161–172. doi: 10.1111/j.1365-313X.2012.04981.x
22. Chen, F., D’Auria, J. C., Tholl, D., Ross, J. R., Gershenzon, J., Noel, J. P., et al. (2003). An Arabidopsis thaliana gene for methylsalicylate biosynthesis, identified by a biochemical genomics approach, has a role in defense. Plant J. 36, 577–588. doi: 10.1046/j.1365-313X.2003.01902.x
23. Chen, J. C., Lu, H. C., Chen, C. E., Hsu, H. F., Chen, H. H., and Yeh, H. H. (2013). The NPR1 ortholog PhaNPR1 is required for the induction of PhaPR1 in Phalaenopsis aphrodite. Bot. Stud. 54, 31. doi: 10.1186/1999-3110-54-31
24. Chen, X. K., Zhang, J. Y., Zhang, Z., Du, X. L., Du, B. B., and Qu, S. C. (2012). Overexpressing MhNPR1 in transgenic Fuji apples enhances resistance to apple powdery mildew. Mol. Biol. Rep. 39, 8083–8089. doi: 10.1007/s11033-012-1655-3
25. Chen, Z., Zheng, Z., Huang, J., Lai, Z., and Fan, B. (2009). Biosynthesis of salicylic acid in plants. Plant Signal. Behav. 4, 493–496. doi: 10.4161/psb.4.6.8392
26. Cheong, H., Kim, C. Y., Jeon, J. S., Lee, B. M., Moon S. J., and Hwang, I. (2013). Xanthomonas oryzae pv. oryzae type III effector XopN targets OsVOZ2 and a putative thiamine synthase as a virulence factor in rice. PLoS ONE 8:e73346. doi: 10.1371/journal.pone.0073346
27. Chern, M., Bai, W., Ruan, D., Oh, T., Chen, X., and Ronald, P. C. (2014). Interaction specificity and coexpression of rice NPR1 homologs 1 and 3 (NH1 and NH3), TGA transcription factors and Negative Regulator of Resistance(NRR) proteins. BMC Genomics 15:461. doi: 10.1186/1471-2164-15-461
28. Chern, M., Fitzgerald, H. A., Canlas, P. E., Navarre, D. A., and Ronald, P. C. (2005). Overexpression of a rice NPR1 homolog leads to constitutive activation of defense response and hypersensitivity to light. Mol. Plant Microbe Interact. 6,511–520. doi: 10.1094/MPMI-18-0511
29. Chern, M. S., Fitzgerald, H. A., Yadav, R. C., Canlas, P. E., Dong, X., and Ronald, P. C. (2001). Evidence for a disease-resistance pathway in rice similar to the NPR1-mediated signaling pathway in Arabidopsis. Plant J. 27, 101–113. doi:10.1046/j.1365-313x.2001.01070.x
30. Coppinger, P., Repetti, P. P., Day, B., Dahlbeck, D., Mehlert, A., and Staskawicz, B. J. (2004). Overexpression of the plasma membrane-localized NDR1 protein results in enhanced bacterial disease resistance in Arabidopsis thaliana. Plant J.40, 225–237. doi: 10.1111/j.1365-313X.2004.02203.x
31. Cui, F., Wu, S., Sun, W., Coaket, G., Kunkel, B., He, P., et al. (2013). The Pseudomonas syringae type III effector AvrRpt2 promotes pathogen virulence via stimulating Arabidopsis auxin/indole acetic acid protein turnover. Plant Physiol. 162, 1018–1029. doi: 10.1104/pp.113.219659
32. Cunnac, S., Lindeberg, M., and Collmer, A. (2009). Pseudomonas syringae type III secretion system effectors: repertoires in search of functions. Curr. Opin. Microbiol. 12, 53–60. doi: 10.1016/j.mib.2008.12.003
33. Dangl, J. L., Dietrich, R. A., and Richberg, M. H. (1996). Death don’t have nomercy:Cell death programs in plant-microbe interactions. Plant Cell 8, 1793–1807. doi:10.1105/tpc.8.10.1793
34. Dangl, J. L., Horvath, D. M., and Staskawicz, B. J. (2013). Pivoting the plant immune system from dissection to deployment. Science 341, 746–751. doi:10.1126/science.1236011
35. Delledonne, M., Xia, Y., Dixon, R. A., and Lamb, C. (1998). Nitric oxide functions as a signal in plant disease resistance. Nature 394, 585–588. doi: 10.1038/29087
36. Dempsey, D. A., and Klessig, D. F. (2012). SOS-too many signals for systemic acquired resistance? Trends Plant Sci. 17, 538–545. doi:10.1016/j.tplants.2012.05.011
37. Dempsey, D. A., Vlot, A. C., Wildermuth, M. C., and Klessig, D. F. (2011).Salicylic acid biosynthesis and metabolism. Arabidopsis Book 9, e0156. doi:10.1199/tab.0156
38. Després, C., DeLong, C., Glaze, S., Liu, E., and Fobert, P. R. (2000). The Arabidopsis NPR1/NIM1 protein enhances the DNA binding activity of a subgroup of the TGA family of bZIP transcription factors. Plant Cell 12, 279–290. doi:10.1105/tpc.12.2.279
39. Dey, S., Wenig, M., Langen, G., Sharma, S., Kugler, K. G., Knappe, C., et al. (2014). Bacteria-triggered systemic immunity in barley is associated with WRKY and ETHYLENE RESPONSIVE FACTORs but not with salicylic acid. Plant Physiol.166, 2133–2151. doi: 10.1104/pp.114.249276
40. Dong, X. (2004). NPR1, all things considered. Curr. Opin. Plant Biol. 7, 547–552. doi: 10.1016/j.pbi.2004.07.005
41. Effmert, U., Saschenbrecker, S., Ross, J., Negre, F., Fraser, C. M., Noel, J. P., et al. (2005). Floral benzenoid carboxyl methyltransferases: from in vitro to in planta function. Phytochemistry 66, 1211–1230. doi: 10.1016/j.phytochem.2005.03.031
42. Ekengren, S. K., Liu, Y., Schiff, M., Dinesh-Kumar, S. P., and Martin, G. B. (2003). Two MAPK cascades, NPR1, and TGA transcription factors play a role in Pto-mediated disease resistance in tomato. Plant J. 36, 905–917. doi:10.1046/j.1365-313X.2003.01944.x
43. El-Shetehy, M., Wang, C., Shine, M. B., Yu, K., Navarre, D., Wendehenne, D., et al. (2015). Nitric oxide and reactive oxygen species are required for systemic acquired resistance in plants. Plant Signal. Behav. In Press.
44. Falk, A., Feys, B. J., Frost, L. N., Jonathan, D. G., Jones, D. G., Michael, J., et al. (1999). EDS1, an essential component of R gene-mediated disease resistance in Arabidopsis has homology to eukaryotic lipases. Proc. Natl. Acad. Sci. U.S.A. 96,3292–3297. doi: 10.1073/pnas.96.6.3292
45. Fan, W., and Dong, X. (2002). In vivo interaction between NPR1 and transcription factor TGA2 leads to salicylic acid-mediated gene activation in Arabidopsis.Plant Cell 14, 1377–1389. doi: 10.1105/tpc.001628
46. Feys, B. J., Moisan, L. J., Newman, M. A., and Parker, J. E. (2001). Direct interaction between the Arabidopsis disease resistance signaling proteins, EDS1 and PAD4.EMBO J. 20, 5400–5411. doi: 10.1093/emboj/20.19.5400
47. Feys, B. J., Wiermer, M., Bhat, R. A., Moisan, L. J., Medina-Escobar, N., Neu, C., et al. (2005). Arabidopsis SENESCENCE-ASSOCIATED GENE101 stabilizes and signals within an ENHANCED DISEASE SUSCEPTIBILITY1 complex in plant innate immunity. Plant Cell 7, 2601–2613. doi: 10.1105/tpc.105.033910
48. Fragnière, C., Serrano, M., Abou-Mansour, E., Métraux, J. P., and L’Haridon, F. (2011). Salicylic acid and its location in response to biotic and abiotic stress. FEBS Lett. 585, 1847–1852. doi: 10.1016/j.febslet.2011.04.039
49. Fu, Z. Q., and Dong, X. (2013). Systemic acquired resistance: turning local infection into global defense. Annu. Rev. Plant Biol. 64, 839–863. doi: 10.1146/annurev-arplant-042811-105606
50. Fu, Z. Q., Yan, S., Saleh, A., Wang, W., Ruble, J., Oka, N., et al. (2012). NPR3 and NPR4 are receptors for the immune signal salicylic acid in plants. Nature 486, 228–232. doi: 10.1038/nature11162
51. Gao, Q. M., Xia, Y., Yu, K., Navarre, D., Kachroo, A., and Kachroo, P. (2014). Galactolipids are required for nitric oxide biosynthesis and systemic acquired resistance. Cell Rep. 9, 1681–1691. doi: 10.1016/j.celrep.2014.10.069
52. García, A. V., Blanvillain-Baufumé, S., Huibers, R. P., Wiermer, M., Li, G., Gobbato, E., et al. (2010). Balanced nuclear and cytoplasmic activities of EDS1 are required for a complete plant innate immune response. PLoS Pathog. 6:e1000970. doi: 10.1371/journal.ppat.1000970
53. Garcion, C., Lohmann, A., Lamodière, E., Catinot, J., Buchala, A., Doermann, P., et al. (2008). Characterization and biological function of the ISOCHORISMATE SYNTHASE2 gene of Arabidopsis. Plant Physiol. 147, 1279–1287. doi: 10.1104/pp.108.119420
54. Giraldo, M., and Valent, B. (2013). Filamentous plant pathogen effectors in action. Nat. Rev. Microbiol. 11, 800–814. doi: 10.1038/nrmicro3119
55. Glazebrook, J. (2005). Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu. Rev. Phytopathol. 43, 205–227. doi: 10.1146/annurev.phyto.43.040204.135923
56. Göhre, V., and Robatzek, S. (2008). Breaking the barriers: microbial effector molecules subvert plant immunity. Annu. Rev. Phytopathol. 46, 189–215. doi: 10.1146/annurev.phyto.46.120407.110050
57. Gruner, K., Griebel, T., Návarová, H., Attaran, E., and Zeier, J. (2013). Reprogramming of plants during systemic acquired resistance. Front. Plant Sci. 4:252. doi: 10.3389/fpls.2013.00252
58. Gu, K., Yang, B., Tian, D., Wu, L., Wang, D., Sreekala, C., et al. (2005). R gene expression induced by a type-III effector triggers disease resistance in rice. Nature 435, 1122–1125. doi: 10.1038/nature03630
59. Guedes, M. E. M., Richmond, S., and Kuc, J. (1980). Induced systemic resistance to anthracnose in cucumber as influenced by the location of the inducer inoculation with Colletotrichum lagenarium and the onset of flowering and fruiting. Physiol. Plant Pathol. 17, 229–233. doi: 10.1016/0048-4059(80)90056-9
60. Heidel, A. J., Clarke, J. D., Antonovics, J., and Dong, X. (2004). Fitness costs of mutations affecting the systemic acquired resistance pathway in Arabidopsis thaliana. Genetics 168, 2197–2206. doi: 10.1534/genetics.104.032193
61. Heidrich, K., Wirthmueller, L., Tasset, C., Pouzet, C., Deslandes, L., and Parker, J. E. (2011). Arabidopsis EDS1 connects pathogen effector recognition to cell compartment-specific immune responses. Science 334, 1401–1404. doi: 10.1126/science.1211641
62. Heil, M., and Baldwin, I. T. (2002). Fitness costs of induced resistance: emerging experimental support for a slippery concept. Trends Plant Sci. 7, 61–66. doi: 10.1016/S1360-1385(01)02186-0
63. Hennig, J., Malamy, J., Grynkiewicz, G., Indulski, J., and Klessig, D. (1993). Interconversion of the salicylic acid signal and its glucoside in tobacco. Plant J. 4, 593–600. doi: 10.1046/j.1365-313X.1993.04040593.x
64. Holliday, M. J., Keen, N. T., and Long, M. (1981). Cell death patterns and accumulation of fluorescent material in the hypersensitive response of soybean leaves to Pseudomonas syringae pv. Glycinea. Physiol. Plant Pathol. 18, 279–287. doi: 10.1016/S0048-4059(81)80079-3
65. Huang, J., Gu, M., Lai, Z., Fan, B., Shi, K., Zhou, Y. H., et al. (2010). Functional analysis of the Arabidopsis PAL gene family in plant growth, development, and response to environmental stress. Plant Physiol. 153, 1526–1538. doi: 10.1104/pp.110.157370
66. Ishihara, T., Sekine, K. T., Hase, S., Kanayama, Y., Seo, S., Ohashi, Y., et al. (2008). Overexpression of the Arabidopsis thaliana EDS5 gene enhances resistance to viruses. Plant Biol. 10, 451–461. doi: 10.1111/j.1438-8677.2008.00050.x
67. Jaskiewicz, M., Conrath, U., and Peterhänsel, C. (2011). Chromatin modification acts as a memory for systemic acquired resistance in the plant stress response. EMBO Rep. 12, 50–55. doi: 10.1038/embor.2010.186
68. Jirage, D., Tootle, T. L., Reuber, T. L., Frost, L. N., Feys, B. J., Parker, J. E., et al. (1999). Arabidopsis thaliana PAD4 encodes a lipase-like gene that is important for salicylic acid signaling. Proc. Natl. Acad. Sci. U.S.A. 96, 13583–13588. doi: 10.1073/pnas.96.23.13583
69. Jones, J. D. G., and Dangl, J. L. (2006). The plant immune system. Nature 444, 323–329. doi: 10.1038/nature05286
70. Jung, H. W., Tschaplinkski, T. J., Wang, L., Glazebrook, J., and Greenberg, J. T. (2009). Priming in systemic plant immunity. Science 324, 89–91. doi: 10.1126/science.1170025
71. Kachroo, A., and Kachroo, P. (2009). Fatty acid-derived signals in plant defense. Annu. Rev. Phytopathol. 47, 153–176. doi: 10.1146/annurev-phyto-080508-081820
72. Kachroo, A., and Robin, G. P. (2013). Systemic signaling during plant defense. Curr. Opin. Plant Biol. 16, 527–533. doi: 10.1016/j.pbi.2013.06.019
73. Kachroo, P., and Kachroo, A. (2012). “The roles of salicylic acid and jasmonic acid in plant immunity,” in Molecular Plant Immunity, ed. G. Sessa (Oxford: Wiley-Blackwell). doi: 10.1002/9781118481431.ch4
74. Kawano, T., Furuichi, T., and Muto, S. (2004). Controlled free salicylic acid levels and corresponding signaling mechanisms in plants. Plant Biotechnol. 21, 319–335. doi: 10.5511/plantbiotechnology.21.319
75. Kiefer, I. W., and Slusarenko, A. J. (2003). The pattern of systemic acquired resistance induction within the Arabidopsis rosette in relation to the pattern of translocation. Plant Physiol. 132, 840–847. doi: 10.1104/pp.103.021709
76. Kim, H. S., and Delaney, T. P. (2002). Over-expression of TGA5, which encodes a bZIP transcription factor that interacts with NIM1/NPR1, confers SAR-independent resistance in Arabidopsis thaliana to Peronospora parasitica. Plant J. 32, 151–163. doi: 10.1046/j.1365-313X.2001.01411.x
77. Kinkema, M., Fan, W., and Dong, X. (2000). Nuclear localization of NPR1 is required for activation of PR gene expression. Plant Cell 12, 2339–2350. doi: 10.1105/tpc.12.12.2339
78. Knepper, C., Savory, E. A., and Day, B. (2011). Arabidopsis NDR1 is an integrin-like protein with a role in fluid loss and plasma membrane-cell wall adhesion. Plant Physiol. 156, 286–300. doi: 10.1104/pp.110.169656
79. Koo, Y. J., Kim, M. A., Kim, E. H., Song, J. T., Jung, C., Moon, J. K., et al. (2007). Overexpression of salicylic acid carboxyl methyltransferase reduces salicylic acid-mediated pathogen resistance in Arabidopsis thaliana. Plant Mol. Biol. 64, 1–15. doi: 10.1007/s11103-006-9123-x
80. Kumar, D., and Klessig, D. F. (2003). High-affinity salicylic acid-binding protein 2 is required for plant innate immunity and has salicylic acid stimulated lipase activity. Proc. Natl. Acad. Sci. U.S.A. 100, 16101–16106. doi: 10.1073/pnas.0307162100
81. Lai, Z., and Mengiste, T. (2013). Genetic and cellular mechanisms regulating plant responses to necrotrophic pathogens. Curr. Opin. Plant Biol. 16, 505–512. doi: 10.1016/j.pbi.2013.06.014
82. Lawton, K., Weymann, K., Friedrich, L., Vernooij, B., Uknes, S., and Ryals, J. (1995). Systemic acquired resistance in Arabidopsis requires salicylic acid but not ethylene. Mol. Plant Microbe Interact. 8, 863–870. doi: 10.1094/MPMI-8-0863
83. Lin, W. C., Lu, C. F., Wu, J. W., Cheng, M. L., Lin, Y. M., Yang, N. S., et al. (2004). Transgenic tomato plants expressing the Arabidopsis NPR1 gene display enhanced resistance to a spectrum of fungal and bacterial diseases. Transgenic Res. 13, 567–581. doi: 10.1007/s11248-004-2375-9
84. Lindermayr, C., Sell, S., Müller, B., Leister, D., and Durner, J. (2010). Redox regulation of the NPR1-TGA1 system of Arabidopsis thaliana by nitric oxide. Plant Cell 22, 2894–2907. doi: 10.1105/tpc.109.066464
85. Liu, G., Holub, E. B., Alonso, J. M., Ecker, J. R., and Fobert, P. R. (2005). An Arabidopsis NPR1-like gene, NPR4, is required for disease resistance. Plant J. 41, 304–318. doi: 10.1111/j.1365-313X.2004.02296.x
86. Liu, P. P., von Dahl, C. C., and Klessig, D. F. (2011). The extent to which methyl salicylate is required for signaling systemic acquired resistance is dependent on exposure to light after infection. Plant Physiol. 157, 2216–2226. doi: 10.1104/pp.111.187773
87. Liu, P. P., Yang, Y., Pichersky, E., and Klessig, D. F. (2010). Altering expression of benzoic acid/salicylic acid carboxyl methyltransferase 1 compromises systemic acquired resistance and PAMP-triggered immunity in Arabidopsis. Mol. Plant Microbe Interact. 23, 82–90. doi: 10.1094/MPMI-23-1-0082
88. Louis, J., Gobbato, E., Mondal, H. A., Feys, B. J., Parker, J. E., and Shah, J. (2012). Discrimination of Arabidopsis PAD4 activities in defense against green peach aphid and pathogens. Plant Physiol. 158, 1860–1872. doi: 10.1104/pp.112.193417
89. Louis, J., Leung, Q., Pegadaraju, V., Reese, J., and Shah, J. (2010). PAD4-dependent antibiosis contributes to the ssi2-conferred hyper-resistance to the green peach aphid. Mol. Plant Microbe Interact. 23, 618–627. doi: 10.1094/MPMI-23-5-0618
90. Lu, H., Zhang, C., Albrecht, U., Shimizu, R., Wang, G., and Bowman, K. D. (2013). Overexpression of a citrus NDR1 ortholog increases disease resistance in Arabidopsis. Front. Plant Sci. 4:157. doi: 10.3389/fpls.2013.00157
91. Lucas, W. J., Groover, A., Lichtenberger, R., Furuta, K., Yadav, S. R., Helariutta, Y., et al. (2013). The plant vascular system: evolution, development and functions. J. Integr. Plant Biol. 55, 294–388. doi: 10.1111/jipb.12041
92. Luna, E., Bruce, T. J., Roberts, M. R., Flors, V., and Ton, J. (2012). Next-generation systemic acquired resistance. Plant Physiol. 158, 844–853. doi: 10.1104/pp.111.187468
93. Mackey, D., Belkhadir, Y., Alonso, J. M., Ecker, J. R., and Dangl, J. L. (2003). Arabidopsis RIN4 is a target of the type III virulence effector AvrRpt2 and modulates RPS2-mediated resistance. Cell 112, 379–389. doi: 10.1016/S0092-8674(03)00040-0
94. Mackey, D., Holt, B. F., Wiig, A., and Dangl, J. L. (2002). RIN4 interacts with Pseudomonas syringae type III effector molecules and is required for RPM1-mediated resistance in Arabidopsis. Cell 108, 743–754. doi: 10.1016/S0092-8674(02)00661-X
95. Malamy, J., Carr, J. P., Klessig, D. F., and Raskin, I. (1990). Salicylic acid: a likely endogenous signal in the resistance response of tobacco to viral infection. Science 250, 1002–1004. doi: 10.1126/science.250.4983.1002
96. Maldonado, A. M., Doerner, P., Dixon, R. A., Lamb, C. J., and Cameron, R. K. (2002). A putative lipid transfer protein involved in systemic resistance signaling in Arabidopsis. Nature 419, 399–403. doi: 10.1038/nature00962
97. Mandal, M. K., Chandra-Shekara, A. C., Jeong, R. D., Yu, K., Zhu, S., Chanda, B., et al. (2012). Oleic acid-dependent modulation of NITRIC OXIDE ASSOCIATED1 protein levels regulates nitric oxide-mediated defense signaling in Arabidopsis. Plant Cell 24, 1654–1674. doi: 10.1105/tpc.112.096768
98. Manohar, M., Tian, M., Moreau, M., Park, S. W., Choi, H. W., Fei, Z., et al. (2015). Identification of multiple salicylic acid-binding proteins using two high throughput screens. Front. Plant Sci. 5:777. doi: 10.3389/fpls.2014.00777
99. Marrtin, F., and Kamoun, S. (2012). Effectors in Plant-microbe Interactions. Chichester; Ames, IA: Wiley-Blackwell.
100. Much-Mani, B., and Slusarenko, A. J. (1996). Production of salicylic acid precursors is a major function of phenylalanine ammonia-lyase in the resistance of Arabidopsis to Peronospora parasitica. Plant Cell 8, 203–212. doi: 10.1105/tpc.8.2.203
101. McDowell, J. M., Cuzick, A., Can, C., Beynon, J., Dangl, J. L., and Holub, E. B. (2000). Downy mildew (Peronospora parasitica) resistance genes in Arabidopsis vary in functional requirements for NDR1, EDS1, NPR1 and salicylic acid accumulation. Plant J. 22, 523–529. doi: 10.1046/j.1365-313x.2000.00771.x
102. Kown, R., Kuroki, G., and Warren, G. (1996). Cold responses of Arabidopsis mutants impaired in freezing tolerance. J. Exp. Bot. 47, 1919–1925. doi: 10.1093/jxb/47.12.1919
103. Mangiste, T. (2012). Plant immunity to necrotrophs. Annu. Rev. Phytopathol. 50, 267–294. doi: 10.1146/annurev-phyto-081211-172955
104. Metraux, J. P., Signer, H., Ryals, J., Ward, E., Wyss-Benz, M., Gaudin, J., et al. (1990). Increase in salicylic acid at the onset of systemic acquired resistance in cucumber. Science 250, 1004–1006. doi: 10.1126/science.250.4983.1004
105. Meuwly, P., and Métraux, J. P. (1993). Ortho-anisic acid as internal standard for the simultaneous quantitation of salicylic acid and its putative biosyn-thetic precursors in cucumber leaves. Anal. Biochem. 214, 500–505. doi: 10.1006/abio.1993.1529
106. Meuwly, P., Molders, W., Buchala, A., and Metraux, J. P. (1995). Local and systemic biosynthesis of salicylic acid in infected cucumber plants. Plant Physiol. 109, 1107–1114.
107. Mishina, T. E., and Zeier, J. (2006). The Arabidopsis flavin-dependent monooxyge-nase FMO1 is an essential component of biologically induced systemic acquired resistance. Plant Physiol. 141, 1666–1675. doi: 10.1104/pp.106.081257
108. Molders, W., Meuwly, P., Summermatter, K., and Métraux, J. P. (1994). Salicylic acid content in cucumber plants infected with Pseudomonas lachrymans and tobacco necrosis virus. Acta Hortic. 381, 375–378.
109. Morel, J. B., and Dangl, J. L. (1997). The hypersensitive response and the induction of cell death in plants. Cell Death Differ. 4, 671–683. doi: 10.1038/sj.cdd.4400309
110. Mou, Z., Fan, W., and Dong, X. (2003). Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes. Cell 113, 935–944. doi: 10.1016/S0092-8674(03)00429-X
111. Narusaka, M., Shirasu, K., Noutoshi, Y., Kubo, Y., Shiraishi, T., Iwabuchi, M., et al. (2009). RRS1 and RPS4 provide a dual Resistance-gene system against fungal and bacterial pathogens. Plant J. 60, 218–226. doi: 10.1111/j.1365-313X.2009.03949.x
112. Návarová, H., Bernsdorff, F., Döring, A. C., and Zeier, J. (2012). Pipecolic acid, an endogenous mediator of defense amplification and priming, is a critical regulator of inducible plant immunity. Plant Cell 24, 5123–5141. doi: 10.1105/tpc.112.103564
113. Nawrath, C., Heck, S., Parinthawong, N., and Metraux, J. P. (2002). EDS5, an essential component of salicylic acid dependent signaling for disease resistance in Arabidopsis, is a member of the MATE transporter family. Plant Cell 14, 275–286. doi: 10.1105/tpc.010376
114. Niggeweg, R., Thurow, C., Kegler, C., and Gatz, C. (2000). Tobacco transcription factor TGA2.2 is the main component of as-1-binding factor ASF-1 and is involved in salicylic acid- and auxin-inducible expression of as-1-containing target promoters. J. Biol. Chem. 275, 19897–19905. doi: 10.1074/jbc.M909267199
115. Pallas, J. A., Paiva, N. L., Lamb, C., and Dixon, R. A. (1996). Tobacco plants epige-netically suppressed in phenylalanine ammonia-lyase expression do not develop systemic acquired resistance in response to infection by tobacco mosaic virus. Plant J. 10, 281–293. doi: 10.1046/j.1365-313X.1996.10020281.x
116. Park, S. W., Kaiyomo, E., Kumar, D., Mosher, S. L., and Klessig, D. F. (2007). Methyl salicylate is a critical mobile signal for plant systemic acquired resistance. Science 318, 113–116. doi: 10.1126/science.1147113
117. Park, S. W., Liu, P. P., Forouhar, F., Vlot, A. C., Tong, L., Tietjen, K., et al. (2009). Use of a synthetic salicylic acid analog to investigate the roles of methyl salicy-late and its esterases in plant disease resistance. J. Biol. Chem. 284, 7307–7317. doi: 10.1074/jbc.M807968200
118. Pegadaraju, V., Knepper, C., Reese, J., and Shah, J. (2005). Premature leaf senescence modulated by the Arabidopsis PHYTOALEXIN DEFICIENT 4 gene is associated with defense against the phloem-feeding green peach aphid1. Plant Physiol. 139, 1927–1934. doi: 10.1104/pp.105.070433
119. Pegadaraju, V., Louis, J., Singh, V., Reese, J. C., Bautor, J., Feys, B. J., et al. (2007). Premature leaf senescence modulated by the Arabidopsis PHYTOALEXIN DEFICIENT4 gene is associated with defense against the phloem-feeding green peach aphid1. Plant J. 52, 332–341. doi: 10.1111/j.1365-313X.2007.03241.x
120. Pierpoint, W. S. (1994). Salicylic acid and its derivatives in plants: medicines, metabolites and messenger molecules. Bot. Res. 20, 163–235. doi: 10.1016/S0065-2296(08)60217-7
121. Rasmussen, J. B., Hammerschmidt, R., and Zook, M. N. (1991). Systemic induction of salicylic acid accumulation in cucumber after inoculation with Pseudomonas syringae pv syringae. Plant Physiol. 97, 1342–1347. doi: 10.1104/pp.97.4.1342
122. Rietz, S., Stamm, A., Malonek, S., Wagner, S., Becker, D., Medina-Escobar, N., et al. (2011). Different roles of enhanced disease susceptibility1 (EDS1) bound to and dissociated from phytoalexin deficient4 (PAD4) in Arabidopsis immunity. New Phytol. 191, 107–119. doi: 10.1111/j.1469-8137.2011.03675.x
123. Rivas-San Vicente, M., and Plasencia, J. (2011). Salicylic acid beyond defence: its role in plant growth and development. J. Exp. Bot. 62, 3321–3338. doi: 10.1093/jxb/err031
124. Sandhu, D., Tasma, I. M., Frasch, R., and Bhattacharyya, M. K. (2009). Systemic acquired resistance in soybean is regulated by two proteins, Orthologous to Arabidopsis NPR1. BMC Plant Biol. 9:105. doi: 10.1186/1471-2229-9-105
125. Schwessinger, B., and Ronald, P. C. (2012). Plant innate immunity: perception of conserved microbial signatures. Annu. Rev. Plant Biol. 63, 451–482. doi: 10.1146/annurev-arplant-042811-105518
126. Serrano, M., Wang, B., Aryal, B., Garcion, C., Abou-Mansour, E., Heck, S., et al. (2013). Export of salicylic acid from the chloroplast requires the MATElike transporter EDS5. Plant Physiol. 162, 1815–1821. doi: 10.1104/pp.113.218156
127. Shah, J. (2003). The salicylic acid loop in plant defense. Curr. Opin. Plant Biol. 6, 365–371. doi: 10.1016/S1369-5266(03)00058-X
128. Shah, J., and Zeier, J. (2013). Long-distance communication and signal amplification in systemic acquired resistance. Front. Plant Sci. 4:30. doi: 10.3389/fpls.2013.00030
129. Shi, Z., Maximova, S. N., Liu, Y., Verica, J., and Guiltinan, M. J. (2010). Functional analysis of the Theobroma cacao NPR1 gene in Arabidopsis. BMC Plant Biol. 10:248. doi: 10.1186/1471-2229-10-248
130. Shimono, M., Sugano, S., Nakayama, A., Jiang, C. J., Ono, K., Toki, S., et al. (2007). Rice WRKY45 plays a crucial role in benzothiadiazole-inducible blast resistance. Plant Cell 19, 2064–2076. doi: 10.1105/tpc.106.046250
131. Shulaev, V., Leon, J., and Raskin, I. (1995). Is salicylic acid a translocated signal of systemic acquired resistance in tobacco? Plant Cell 7, 1691–1701. doi: 10.1105/tpc.7.10.1691
132. Singh, V., Roy, S., Giri, M. K., Chaturvedi, R., Chowdhury, Z., Shah, J., et al. (2013). Arabidopsis thaliana FLOWERING LOCUS D is required for systemic acquired resistance. Mol. Plant Microbe Interact. 26, 1079–1088. doi: 10.1094/MPMI-04-13-0096-R
133. Song, F., and Goodman, R. M. (2001). Activity of nitric oxide is dependent on, but is partially required for function of, salicylic acid in the signaling pathway in tobacco systemic acquired resistance. Mol. Plant Microbe Interact. 14, 1458–1462. doi: 10.1094/MPMI.2001.14.12.1458
134. Song, J. T., Lu, H., McDowell, J. M., and Greenberg, J. T. (2004a). A key role for ALD1 in activation of local and systemic defenses in Arabidopsis. Plant J. 40, 200–212. doi: 10.1111/j.1365-313X.2004.02200.x
135. Song, J., Lu, H., and Greenberg, J. (2004b). Divergent roles in Arabidopsis thaliana development and defense of two homologous genes, ABERRANT GROWTH AND DEATH2 and AGD2-LIKE DEFENSE RESPONSE PROTEIN1, encoding novel aminotransferases. Plant Cell 16, 353–366. doi: 10.1105/tpc.019372
136. Spoel, S., and Dong, X. (2012). How do plants achieve immunity? Defence withoug specialized immune cells. Nat. Rev. Immunol. 12, 89–100. doi: 10.1038/nri3141
137. Spoel, S. H., Mou, Z., Tada, Y., Spivey, N. W., Genschik, P., and Dong, X. (2009). Proteasome-mediated turnover of the transcription coactivator NPR1 plays dual role in regulating plant immunity. Cell 137, 860–872. doi: 10.1016/j.cell.2009.03.038
138. Strawn, M. A., Marr, S. K., Inoue, K., Inada, N., Zubieta, C., and Wildermuth, M. C. (2007). Arabidopsis isochorismate synthase functional in pathogen-induced salicylate biosynthesis exhibits properties consistent with a role in diverse stress responses. J. Biol. Chem. 282, 5919–5933. doi: 10.1074/jbc.M605193200
139. Tada, Y., Spoel, S. H., Pajerowska-Mukhtar, K., Mou, Z., Song, J., Wang, C., et al. (2008). Plant immunity requires conformational changes of NPR1 via S-nitrosylation and thioredoxins. Science 321, 952–956. doi: 10.1126/sci-ence.1156970
140. Truman, W. M., Bennett, M. H., Turnbull, C. G., and Grant, M. R. (2010). Arabidopsis auxin mutants are compromised in systemic acquired resistance and exhibit aberrant accumulation of various indolic compounds. Plant Physiol. 152, 1562–1573. doi: 10.1104/pp.109.152173
141. Truman, W., and Glazebrook, J. (2012). Co-expression analysis identifies putative targets for CBP60g and SARD1 regulation. BMC Plant Biol. 12:216. doi: 10.1186/1471-2229-12-216
142. Tuzun, S., and Kuc, J. (1985). Movement of a factor in tobacco infected with Peranospora tabacina Adam which systemically protects against blue mold. Physiol. Plant Pathol. 26, 321–330. doi: 10.1016/0048-4059(85)90007-4
143. Ung, H., Moeder, W., and Yoshioka, K. (2014). Arabidopsis triphosphate tunnel metalloenzyme2 is a negative regulator of the salicylic acid-mediated feedback amplification loop for defense responses. Plant Physiol. 166, 1009–1021. doi: 10.1104/pp.114.248757
144. Uzunova, A. N., and Popova, L. P. (2000). Effect of salicylic acid on leaf anatomy and chloroplast ultrastructure of barley plants. Photosynthetica 38, 243–250. doi: 10.1023/A:1007226116925
145. Venugopal, S. C., Jeong, R. D., Mandal, M., Zhu, S., Chandra-Shekara, A. C., Xia, Y., et al. (2009). ENHANCED DISEASE SUSCEPTIBILITY and salicylic acid act redundantly to regulate resistance gene-mediated signaling. PLoS Genet. 5:e1000545. doi: 10.1371/journal.pgen.1000545
146. Vernooij, B., Friedrich, L., Morse, A., Reist, R., Kolditz-Jawhar, R., Ward, E., et al. (1994). Salicylic acid is not the translocated signal responsible for inducing systemic acquired resistance but is required in signal transduction. Plant Cell 6, 959–965. doi: 10.1105/tpc.6.7.959
147. Vlot, A. C., Dempsey, D. A., and Klessig, D. F. (2009). Salicylic Acid, a multi-faceted hormone to combat disease. Annu. Rev. Phytopathol. 47, 177–206. doi:10.1146/annurev.phyto.050908.135202
148. Wang, C., El-Shetehy, M., Shine, M. B., Yu, K., Navarre, D., Wendehenne, D., et al. (2014a). Free radicals mediate systemic acquired resistance. Cell Rep. 7, 348–355 doi: 10.1016/j.celrep.2014.03.032
149. Wang, J., Shine, M. B., Gao, Q. M., Navarre, D., Jiang, W., Liu, C., et al. (2014b). Enhanced Disease Susceptibility1 mediates pathogen resistance and virulence function of a bacterial effector in soybean. Plant Physiol. 165, 1269–1284. doi:10.1104/pp.114.242495
150. Wang, D., Amornsiripanitch, N., and Dong, X. (2006). A genomic approach to identify regulatory nodes in the transcriptional network of systemic acquired resistance in plants. PLoS Pathog. 2:e123. doi: 10.1371/journal.ppat.0020123
151. Wang, W., Barnaby, J. Y., Tada, Y., Li, H., Tör, M., Caldelari, D., et al. (2011). Timing of plant immune responses by a central circadian regulator. Nature 470, 110–114. doi: 10.1038/nature09766
152. Warren, G., McKown, R., Marin, A., and Teutonico, R. (1996). Isolation of mutations affecting the development of freezing tolerance in Arabidopsis thaliana (L.) Heynh. Plant Physiol. 111, 1011–1019. doi: 10.1104/pp.111.4.1011
153. Wendehenne, D., Gao, Q. M., Kachroo, A., and Kachroo, P. (2014). Free radical-mediated systemic immunity in plants. Curr. Opin. Plant Biol. 20, 127–134. doi: 10.1016/j.pbi.2014.05.012
154. Wildermuth, M. C., Dewdney, J., Wu, G., and Ausubel, F. M. (2001). Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature 414, 562–565. doi: 10.1038/35107108
155. Wink, D. A., Hines, H. B., Cheng, R. Y. S., Switzer, C. H., Flores-Santana, W., Vitek, M. P., et al. (2011). Nitric oxide and redox mechanisms in the immune response. J. Leukoc. Biol. 89, 873–891. doi: 10.1189/jlb.1010550
156. Wittek, F., Hoffmann, T., Kanawati, B., Bichlmeier, M., Knappe, C., Wenig, M., et al. (2014). Arabidopsis ENHANCED DISEASE SUSCEPTIBILITY1 promotes systemic acquired resistance via azelaic acid and its precursor 9-oxo nonanoic acid. J. Exp. Bot. 65, 5919–5931. doi: 10.1093/jxb/eru331
157. Wu, Y., Zhang, D., Chu, J. Y., Boyle, P., Wang, Y., Brindle, I. D., et al. (2012). The Arabidopsis NPR1 protein is a receptor for the plant defense hormone salicylic acid. Cell Rep. 6, 639–647. doi: 10.1016/j.celrep.2012.05.008
158. Xia, Y., Gao, Q. M., Yu, K., Navarre, D., Hildebrand, D., Kachroo, A., et al. (2009). An intact cuticle in distal tissues is essential for the induction of systemic acquired resistance in plants. Cell Host Microbe. 5, 151–165. doi:10.1016/j.chom.2009.01.001
159. Xia, Y., Yu, K., Gao, Q. M., Wilson, E. V., Navarre, D., Kachroo, P., et al. (2012). Acyl CoA binding proteins are required for cuticle formation and plant responses to microbes. Front. Plant Sci. 3:224. doi: 10.3389/fpls.2012.00224
160. Xia, Y., Yu, K., Navarre, D., Seebold, K., Kachroo, A., and Kachroo, P. (2010). The glabra1 mutation affects cuticle formation and plant responses to microbes. Plant Physiol. 154, 833–846. doi: 10.1104/pp.110.161646
161. Yalpani, N., Leon, J., Lawton, M. A., and Raskin, I. (1993). Pathway of salicylic acid biosynthesis in healthy and virus-inoculated tobacco. Plant Physiol. 103, 315–321.
162. Yalpani, N., Silverman, P., Wilson, T. M., Kleier, D. A., and Raskin, I. (1991). Salicylic acid is a systemic signal and an inducer of pathogenesis-related proteins in virus-infected tobacco. Plant Cell 3, 809–818. doi: 10.1105/tpc.3.8.809
163. Yu, J., Gao, J., Wang, X. Y., Wei, Q., Yang, L. F., Qiu, K., et al. (2010). The pathway and regulation of salicylic acid biosynthesis in probenazole-treated Arabidopsis. J. Plant Biol.53, 417–424. doi: 10.1007/s12374-010-9130-y
164. Yu, K., Soares, J. M., Mandal, M. K., Wang, C., Chanda, B., Gifford, A. N., et al. (2013). A feedback regulatory loop between G3P and lipid transfer proteins DIR1 and AZI1 mediates azelaic-acid-induced systemic immunity. Cell Rep. 3, 1266–1278. doi: 10.1016/j.celrep.2013.03.030
165. Yuan, Y., Zhong, S., Li, Q., Zhu, Z., Lou, Y., Wang, L., et al. (2007). Functional analysis of rice NPR1-like genes reveals that OsNPR1/NH1 is the rice orthologue conferring disease resistance with enhanced herbivore susceptibility. Plant Biotechnol. J. 5, 313–324. doi: 10.1111/j.1467-7652.2007.00243.x
166. Zhang, K., Halitschke, R., Yin, C., Liu, C. J., and Gan, S. S. (2013). Salicylic acid 3-hydroxylase regulates Arabidopsis leaf longevity by mediating salicylic acid catabolism. Proc. Natl. Acad. Sci. U.S.A. 110, 14807–14812. doi: 10.1073/pnas.1302702110
167. Zhang, X., Wang, C., Zhang, Y., Sun, Y., and Mou, Z. (2012). The Arabidopsis mediator complex subunit16 positively regulates salicylate-mediated systemic acquired resistance and jasmonate/ethylene-induced defense pathways. Plant Cell 24, 4294–4309. doi: 10.1105/tpc.112.103317
168. Zhang, Y., Cheng, Y. T., Qu, N., Zhao, Q., Bi, D., and Li, X. (2006). Negative regulation of defense responses in Arabidopsis by two NPR1 paralogs. Plant J. 48, 647–656. doi: 10.1111/j.1365-313X.2006.02903.x
169. Zhang, Y., Fan, W., Kinkema, M., Li, X., and Dong, X. (1999). Interaction of NPR1 with basic leucine zipper protein transcription factors that bind sequences required for salicylic acid induction of the PR-1 gene. Proc. Natl. Acad. Sci. U.S.A. 96, 6523–6528. doi: 10.1073/pnas.96.11.6523
170. Zhang, Y., Tessaro, M. J., Lassner, M., and Li, X. (2003). Knockout analysis of Arabidopsis transcription factors TGA2, TGA5, and TGA6 reveals their redundant and essential roles in systemic acquired resistance. Plant Cell 15, 2647–2653. doi: 10.1105/tpc.014894
171. Zhang, Y., Xu, S., Ding, P., Wang, D., Cheng, Y. T., He, J., et al. (2010). Control of salicylic acid synthesis and systemic acquired resistance by two members of a plant-specific family of transcription factors. Proc. Natl. Acad. Sci. U.S.A. 107, 18220–18225. doi: 10.1073/pnas.1005225107
172. Zhou, J. M., Trifa, Y., Silva, H., Pontier, D., Lam, E., Shah, J., et al. (2000). NPR1 differentially interacts with members of the TGA/OBF family of transcription factors that bind an element of the PR-1 gene required for induction by salicylic acid. Mol. Plant Microbe Interact. 13, 191–202. doi: 10.1094/MPMI.2000.13.2.191
173. Zhu, S., Jeong, R. D., Venugopal, S. C., Lapchyk, L., Navarre, D., Kachroo, A., et al. (2011). SAG101 forms a ternary complex with EDS1 and PAD4 and is required for resistance signaling against Turnip crinkle virus. PLoS Pathog. 7:e1002318. doi: 10.1371/journal.ppat.1002318
174. Zoeller, M., Stingl, N., Krischke, M., Fekete, A., Waller, F., Berger, S., et al. (2012). Lipid profiling of the Arabidopsis hypersensitive response reveals specific lipid peroxidation and fragmentation processes: biogenesis of pimelic and azelaic acid. Plant Physiol. 160, 365–378. doi: 10.1104/pp.112.202846
175. Zwicker, S., Mast, S., Stos, V., Pfitzner, A. J., and Pfitzner, U. M. (2007). Tobacco NIMIN2 proteins control PR gene induction through transient repression early in systemic acquired resistance. Mol. Plant Pathol. 4, 385–400. doi: 10.1111/j.1364-3703.2007.00399.x